Different Roles of Neurons B63 and B34 That Are Active During the Protraction Phase of Buccal Motor Programs inAplysia californica

Abstract

The buccal ganglion of Aplysia contains a central pattern generator (CPG) that organizes sequences of radula protraction and retraction during food ingestion and egestion. Neurons B63 and B34 have access to, or are elements of, the CPG. Both neurons are depolarized along with B31/B32 during the protraction phase of buccal motor programs. Both cells excite the contralateral B31/B32 neurons and inhibit B64 and other neurons active during the retraction phase. B63 and B34 also both have an axon exiting the buccal ganglia via the contralateral cerebrobuccal connective. Despite their similarities, B63 and B34 differ in a number of properties, which reflects their different functions. B63 fires during both ingestion and egestion-like buccal motor programs, whereas B34 fires only during egestion-like programs. The bilateral B63 neurons, along with the bilateral B31 and B32 neurons, act as a single functional unit. Sufficient depolarization of any of these neurons activates them all and initiates a buccal motor program. B63 is electrically coupled to both the ipsilateral and the contralateral B31/B32 neurons but monosynaptically excites the contralateral neurons with a mixed electrical and chemical excitatory postsynaptic potential (EPSP). Positive feedback caused by electrical and chemical EPSPs between B63 and B31/B32 contributes to the sustained depolarization in B31/B32 and the firing of B63 during the protraction phase of a buccal motor program. B34 is excited during the protraction phase of all buccal motor programs, but, unlike B63, it does not always reach firing threshold. The neuron fires in response to current injection only after it is depolarized for 1-2 s or after preceding buccal motor programs in which it is depolarized. Firing of B34 produces facilitating EPSPs in the contralateral B31/B32 and B63 neurons and can initiate a buccal motor program. Firing in B34 is strongly correlated with firing in the B61/B62 motor neurons, which innervate the muscle (I2) responsible for much of protraction. B34 monosynaptically excites these motor neurons. B34 firing is also correlated with firing in motor neuron B8 during the protraction phase of a buccal motor program. B8 innervates the I4 radula closer muscle, which in egestion movements is active during protraction and in ingestion movements is active during retraction. B34 has a mixed, but predominantly excitatory, effect on B8 via a slow conductance-decrease EPSP. Thus firing in B34 leads to amplification of radula protraction that is coupled with radula closing, a pattern characteristic of egestion.

Identification and Characterization of the Feeding Circuit-Activating Peptides, a Novel Neuropeptide Family ofAplysia

“…FCAP-containing neurons and processes could be observed in the buccal and cerebral ganglia and the gut. Furthermore, both MALDI and IMM detected FCAPs in the CBC, a nerve that contains axons of CBIs and BCIs, two classes of neurons that are implicated in initiation and modulation of feeding motor programs (Rosen et al, 1991;Teyke et al, 1993;Hurwitz et al, 1997Hurwitz et al, , 1999Xin et al, 1999;Sanchez and Kirk, 2000;Jing and Weiss, 2001). We showed that FCAPs are present in several CBIs and BCIs, although the identity of these CBIs and BCIs remains to be defined.…”

“…These neurons include the cerebral-buccal interneurons (CBIs) and buccal-cerebral interneurons (BCIs), which are known to be involved in generating and shaping the cerebral and buccal ganglion-mediated components of feeding motor programs (Rosen et al, 1991;Teyke et al, 1993;Hurwitz et al, 1997;Perrins and Weiss, 1998;Xin et al, 1999). Modulators that can alter feeding motor program output have been localized to some of the known CBIs and BCIs, and evidence suggests that additional, as yet unidentified neuropeptides are present in the feeding circuitry (Lloyd, 1989;Li et al, 1998).…”

Complementary Interactions between Command-Like Interneurons that Function to Activate and Specify Motor Programs

“…A Grass model S88 stimulator was used for stimulation. In addition to CBI-11 (Wu et al, 2003), all other neurons were identified as described previously (Rosen et al, 1991;Hurwitz et al, 1994;Hurwitz and Susswein, 1996;Weiss, 2001, 2002;Sasaki et al, 2009).…”

“…Regardless of the type of motor program, the phasing of the protractionretraction sequence remains constant. Protraction was monitored by recording from the I2 nerve, which contains the axons of protractor motor neurons B31/32 and B61/62 (Hurwitz et al, 1994). In some experiments, retraction was monitored by recording from retraction interneuron B64 (Hurwitz and Susswein, 1996).…”

“…The intertrial interval between stimulations was set to 20 -50 s. CPG activity was monitored via intracellular recordings from the radula protraction motor neuron B61, and the radula closing motor neuron B8. Additionally, we used extracellular recordings from the I2 nerve to monitor aggregate activity of protraction motor neurons B61 and B31 (Hurwitz et al, 1994). Group data show that prestimulation of CBI-2 enhanced the ability of CBI-11 to induce CPG activity: the average B61 burst frequency (F (2,4) ϭ 30.1, p Ͻ 0.01, n ϭ 3; Fig.…”